The non-foliar hypoxic photosynthetic syndrome: evidence for enhanced pools and functionality of xanthophyll cycle components and active cyclic electron flow in fruit chlorenchyma

Main conclusion Green fruits display a high engagement in CEF and enhanced VAZ cycle activity as a response to the demands imposed by their internal aerial conditions, particularly low O₂, due to gas exchange limitations. In the present study, we used HPLC analysis, post-illumination changes in fluorescence yield under varying O₂ and CO₂ partial pressures and absorbance changes at 820 nm induced by far-red light to assess the carotenoid composition, the functionality of the xanthophyll cycle (VAZ) and the possibility of an active cyclic e⁻ flow (CEF) in the fully exposed green fruits from Nerium oleander and Rosa sp. Equally exposed, mature leaves served as controls. Compared to leaves, fruits display less total chlorophylls and carotenoids but higher Car/Chi ratio, mainly shaped by the increased pools of the VAZ cycle components, in both species. The enhanced VAZ pool size in fruits is combined with a higher mid-day de-epoxidation state (DEPS). Moreover, fruits exhibit considerably lower levels of oxidizable P₇₀₀, a faster re-reduction of PSI and significantly higher relative magnitude of CEF, irrespective of the O₂/CO₂ levels applied. We conclude that the higher VAZ investment may serve the enhanced heat dissipation needs in fruits, in the presence of a suppressed linear e⁻ flow. In addition, the elevated potential of CEF may replenish the ATP lost due to hypoxia and concurrently facilitate the development of adequate non-photochemical quenching (NPQ), through its contribution to ∆pH increase. Since other non-foliar green organs exhibit a similar photosynthetic pattern, we argue that this may reflect a common strategy for green tissues under similar micro-environmental conditions, particularly hypoxia.